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Iran Red Crescent Med J. In Press(In Press):e68913. doi: 10.5812/ircmj.68913.

Published online 2018 December 17. Research Article

Comparing the Effectiveness of Vestibular Rehabilitation and Frenkel


Exercise on Fatigue Reduction in Patients with Multiple Sclerosis: A
Randomized Controlled Trial
Fatemeh Karami 1 , Ardashir Afrasiabifar 1, * and Shahla Najafi Doulatabad 1
1
Yasuj University of Medical Sciences, Yasuj, Iran
*
Corresponding author: Yasuj University of Medical Sciences, Yasuj, Iran. Email: afrasiabifar.ardashir@yums.ac.ir

Received 2018 March 26; Revised 2018 October 09; Accepted 2018 October 11.

Abstract

Background: Fatigue is one of the most common complaints in people with Multiple Sclerosis (MS). The use of non-
pharmacological interventions, such as exercise, may be effective in reducing fatigue in these patients.
Objectives: This study aimed to evaluate the effect of vestibular rehabilitation and Frenkel exercise on fatigue in patients with
multiple sclerosis.
Methods: This study was a controlled randomized clinical trial. Seventy-five patients, who had medical records at the society of
special diseases of the Yasuj University of Medical Sciences, Iran, in 2016, were randomly assigned to three groups, namely, vestibular
rehabilitation, Frenkel, and control. The program lasted for 12 weeks (three sessions per week). Fatigue was measured by the Fatigue
Impact Scale (FIS) before the intervention, and after that, at six and twelve weeks after the initiation of intervention.
Results: The mean score of fatigue in both experimental groups was decreased in a statistically significant manner after the end of
the exercises, whereas it was increased in the control group. The reduction in fatigue was statistically significant in the vestibular
rehabilitation exercise in comparison with the Frenkel exercise. The total fatigue in the vestibular rehabilitation group at six and
twelve weeks after the intervention was -14.1 and -33.1, respectively, in comparison with before the interventions yet in the Frenkel
group it was reported as -8 and -17.9, respectively. The comparison of the FIS subscales showed that there was a difference between
the vestibular rehabilitation and Frenkel group in both the FIS physical (P = 0.001) and the psychosocial subscales (P = 0.01), yet no
difference was observed between the two groups in the FIS cognitive subscale (P = 0.1) at twelve weeks after the intervention.
Conclusions: Both vestibular rehabilitation and Frenkel exercise could reduce fatigue in MS patients, however, vestibular rehabili-
tation was more effective compared to the Frenkel exercise in reducing fatigue.

Keywords: Exercise, Fatigue, Frenkel, Multiple Sclerosis, Rehabilitation, Vestibular

1. Background non-pharmacological interventions are considered as ap-


proaches for fatigue management (8). The review of the
Fatigue is defined as a decrease in physical and/or men- literature shows that biofeedback (9) and cognitive behav-
tal performance (1). It is one of the common complaints of ioral therapy (10) have been used to reduce fatigue in MS
patients with Multiple Sclerosis (MS). Seventy-four percent patients.
of such patients suffer from severe fatigue (2) and 80% ex-
perience fatigue in the first year of the onset of MS (3). Fa- Exercise therapy is a non-pharmacological method,
tigue may be the result of hypothalamic-pituitary-adrenal whose impact on MS symptoms has been investigated in
axis changes, immune dysfunctions, and impaired nerve previous studies (11, 12). It was previously thought that exer-
conduction (4). Fatigue can affect all aspects of quality of cise leads to worsening of MS symptoms, in contrast, how-
life (5) of MS patients. ever, recent studies have revealed evidence to support that
Some medications, such as Amantadine, Levocarni- exercise is helpful for MS patients. Exercise can improve
tine, Glatiramer acetate (6), and Natalizumab (7) may balance (13), mental functioning (14), and quality of life
be useful in reducing fatigue of MS patients; however, (15). Although the benefits of exercise are clear, some stud-
there are no known drugs with fewer side effects that ies have shown that MS patients have a lower tendency to
can completely prevent or improve fatigue. Therefore, engage in an exercise in comparison with patients of other

Copyright © 2018, Author(s). This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License
(http://creativecommons.org/licenses/by-nc/4.0/) which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly
cited
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Karami F et al.

chronic diseases (16, 17). There is also no consensus about 3. Methods


the effects of exercise therapy on fatigue in MS patients.
Some studies have reported the positive effects of exercise 3.1. Patients
on fatigue (18, 19); however, the ineffectiveness of exercise This study involved a controlled randomized clinical
on fatigue has also been reported in some studies (20). trial. The population of the study included MS patients,
There are different therapeutic exercises, among who had medical records at the Society of Special Diseases
which simple exercises, such as vestibular rehabilitation of Yasuj University of Medical Sciences, Iran, during the
and Frenkel exercise, should be noted. Vestibular reha- year 2016. The inclusion criteria for patients consisted of
bilitation exercise compensates defects in the vestibular a confirmed diagnosis of disease by a neurologist, pass-
system via adaptation, habituation, and substitution (21), ing at least six months from the onset, being in the re-
and thereby improves the performance of the cerebellar mission period, being between the ages of 15 and 55 years,
and visual system, and ultimately, the individual’s balance ability to stand for 30 seconds, and to walk a distance of
(22). In one study, balance improvement was reported six meters without any assistance, to have a Fatigue Im-
after patients with unilateral vestibular deficit underwent pact Scale (FIS) score from 54 to 107, no history of participa-
a vestibular rehabilitation exercise (23). Frenkel is a type tion in a rehabilitation program within the last six months,
of aerobic exercise that corrects motor defects in the and no diseases other than MS. Furthermore, the patients
cerebellum, stimulate voluntary movement control, and were evaluated by the Berg Balance Scale (BBS) to deter-
helps the Central Nervous System (CNS) compensate the mine the existence of imbalance in these patients before
loss of the kinesthetic sense or the body sensory infor- the intervention. The patients, who had a BBS score from
mation (knowing where it is in space) (24). It includes a 21 to 40 or a moderate imbalance, were selected. Refus-
series of slow, repetitious motions that are performed in ing to continue participation or inability to participate in
different positions when lying down, sitting, and stand- exercises, and the relapse of diseases during the period
ing, and these programs target the cerebellum as the of study were considered as exclusion criteria. Written
main center for controlling balance, and finally lead to informed consent was obtained before starting the exer-
an improvement in balance. In a case report study, the cises. Emphasis was placed on the confidentiality of infor-
improvement of balance in a patient diagnosed with mation, and the patient’s ability to exit at any stage dur-
acquired immunodeficiency syndrome, associated with ing the study. The study was approved by the Research
progressive multifocal leukoencephalopathy and neuro- Ethics Committee of Yasuj University of Medical Sciences
toxoplasmosis, was reported after a year of performing (ETH number: ir.yums.REC.1394.180), and was registered on
Frenkel exercise (25). Since fatigue is considered as the site with the Iranian Registry Clinical Trials with IRCT, num-
predictor of maintenance of somatic balance (26), it seems ber; IRCT2016031527063N1 (29).
that patients, who attempt to maintain balance during the From the 120 available patients, a total of 75 eligible pa-
performance of tasks may experience significant levels of tients with multiple sclerosis, who met the inclusion crite-
fatigue (27). Therefore, balance improvement, following ria, were selected using the convenience sampling method
these exercises, may be useful in reducing fatigue. and were allocated to two groups, vestibular rehabilita-
Since the prevalence of fatigue is high in MS patients tion, and Frenkel exercises, as well as a control group,
and fatigue may be a sign of imbalance (28), and because based on block randomization. The sample size was cal-
of the lack of consensus on the impact of therapeutic exer- culated based on prior studies considering 95% confidence
cises on fatigue, and the limitation of evidence indicating level, 80% power, S1 = 1.3, S2 = 1.4, and µ1 - µ2 = 2.5. The below
the effectiveness of intervention using vestibular rehabili- formula was used:
h i
tation and Frenkel exercise on fatigue in MS patients, fur- S12 + S22

2 Z1− α2 + Z1−β
ther studies in this area are needed. n=
(µ1 − µ2 )2
The randomization process was performed by a per-
2. Objectives son, who was not involved in any part of the study proce-
dure. The groups were randomly labeled (A = vestibular
The main question of this study is whether perform- rehabilitation group, B = Frenkel group, and C = control
ing vestibular rehabilitation and Frenkel exercise could re- group). Since there were three groups in this study, the to-
duce fatigue as well as if there is any difference between tal number of blocks was six in blocks of three. Random
the effectiveness of these exercises. This study was con- sampling with replacement was made from these blocks.
ducted to compare the effect of vestibular rehabilitation, During the intervention, one patient from the Frenkel ex-
and Frenkel exercise on fatigue in MS patients. ercise group dropped out due to disease relapse.

2 Iran Red Crescent Med J. In Press(In Press):e68913.


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Karami F et al.

Furthermore, one patient from the vestibular rehabil- 3.4. Data Analysis
itation group and one patient from the Frenkel exercise
group dropped out of treatment due to being unable to The collected data were analyzed using descriptive
regularly participate. There was no possibility of replace- and inferential statistics, employing the IBM SPSS Statis-
ment because two months had passed since the starting tics Software for Windows, version 19.0 (IBM Corp., Ar-
of the exercises and due to the absence of another eligible mork, N.Y. USA) by considering a confidence interval of
sample. Finally, a total of 72 patients completed the study 95%. At first, the distribution of fatigue was assessed by
(Figure 1). the Kolmogorov-Smirnov Z-test. It had a normal distribu-
tion, therefore, the results of the parametric tests were re-
ported for analysis. A Repeated-Measure Analysis of Vari-
3.2. Procedure ance (ANOVA) was used to compare the mean score of fa-
tigue among the three groups. Since the assumption of
Patients of both intervention groups had participated Mauchly’s test of sphericity of repeated measures ANOVA
in exercise sessions that were held in the outpatient clinic test was violated, Greenhouse Geisser epsilon correction
of Shahid Beheshti Hospital during three exercise sessions, was reported. The mean difference of fatigue was signif-
on alternate days, for a total span of 12 weeks. Each session icant; therefore, pairwise comparison of the mean differ-
lasted for about 60 minutes (Two 30-minute sessions with ence was conducted by Bonferroni post hoc test. Because
15-minute rest intervals). The vestibular rehabilitation ex- there were three groups in this study, the significance level
ercise was performed based on the protocols established was equal to or less than 0.015 (α/3) in the pairwise com-
by Cawthorne and Cooksey. On the basis of the aforemen- parison.
tioned protocols, it was performed in both the sitting and
the upright position; it was performed once with open eyes
and then, the exercise was carried out with closed eyes (30, 4. Results
31). The protocol is described in details in Appendix 1 in
Supplementary File. Seventy-two patients aged between 18 and 48 years
Patients in the Frenkel group performed exercises (Mean: 32.7 ± 7.4) participated in this study. About 56
based on protocols obtained from a previous study (32). (77.8%) patients were female, 68 (94.4%) patients had the
Frenkel exercise was performed in the following different relapsing-remitting type of MS, and four (5.6 %) patients
positions, including lying down, sitting up, and standing had primary and secondary progressive type of MS. Forty-
(Appendix 2 in Supplementary File for details). Patients in two (58.4%) patients used the interferon Beta-1a drug, 16 pa-
the control group only received routine care. tients (22.2%) used the interferon Beta-1b, and the other pa-
tients used other drugs. The mean body mass index, the
age of disease onset, and the duration of illness were 23.4 ±
3.3. Measures 2.3 kg/m2 , 27.6 ± 7.2 years, and 60.5 ± 37.4 months, respec-
tively. No statistically significant difference was observed
Patients’ fatigue was assessed by the Fatigue Impact among the three groups by the demographic variables (P =
Scale (FIS) before the exercises, six and twelve weeks after 0.7).
the start of exercises. The FIS was designed by Fisk et al. Repeated measures ANOVA test showed statistically
to assess fatigue in MS patients (33). This scale contains significant differences in the mean the total fatigue scores
40 items, and assesses the functional limitations of peo- and its subscales in terms of time/group among the three
ple in subscales of categories: Cognitive (10 items), phys- groups (P < 0.05) (Table 1). Pairwise comparison of the
ical (10 items), and psychosocial (20 items). Items of the mean difference of the total fatigue and its subscales
cognitive subscale measure concentration, memory, think- scores showed that there were statistically significant dif-
ing, and the organization of thoughts. The physical sub- ferences between the three groups at the baseline and
scale reflects a person’s motivation, effort, tolerance, and six weeks after starting the intervention (P > 0.05), ex-
harmony. The psychosocial subscale evaluates the impact cept in case of vestibular rehabilitation and in the control
of fatigue upon isolation, emotions, workload, and coping. group, in which pair-wise comparison for six weeks post-
Items are rated on a five-point Likert scale. Each item is intervention was significant (P = 0.009). A statistically sig-
graded from zero (no problem) to four (extreme problem), nificant difference was observed between the vestibular re-
and the range of the total fatigue score is 0 to 160. The va- habilitation and the Frenkel groups at the end of the in-
lidity and the reliability of the Persian version of FIS have tervention (P = 0.007). Comparing the FIS subscales be-
been confirmed previously (34). tween the vestibular rehabilitation and the Frenkel groups

Iran Red Crescent Med J. In Press(In Press):e68913. 3


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Karami F et al.

Assessed for eligibility (n = 120)

Excluded (n = 45)
Not Meeting Inclusion Criteria (n = 38)
10 = Not able to stand independently for 30
seconds
First data gathering (before intervention) 11 = Not able to walk independently a
Enrollment distance of 6 meters
5 = Have a Fatigue Impact Scale (FIS) scores
of less than 54 or more than 107
8 = Have a Berg Balance Scale (BBS) scores
of less than 21 or more than 40
4 = Disease affecting the central nervause
system other than multiple sclerosis
Randomized (n = 75) Declined to Participate (n = 7)

Allocation

Vestibulur rehabilitation (n = 25) Frenkel Group (n = 25) Control Group (n = 25)


Recived allocated intervention Received allocated intervention Received allocated intervention
(n = 25) (n = 25) (n = 25)
Did not receive allocated Did not receive allocated Did not receive allocated
intervention (n = 0) intervention (n = 0) intervention (n = 0)

Follow-Up

Second data gathering ( six weeks after baseline)

Follow-Up

Lost to follow-up after eight weeks Lost to follow-up after eight weeks Lost to follow-up (n = 0)
intervention (n = 1) intervention (n = 2)
Unable to regularly participation Unable to regularly participation
(n = 1) (n = 1)
Disease relapses (n = 1)

Follow-Up

Third data gatherug (twelve weeks After baseline)

Analysis

Analyzed (n = 24) Analyzed (n = 23) Analyzed (n = 25)

Figure 1. The study design

showed that there was no difference in the cognitive sub- ison with Frenkel exercise. The mean total fatigue in the
scale (P = 0.1); significant differences were, however, ob- vestibular rehabilitation group was 92.7 ± 12.8, 78.2 ± 15.2,
served by the physical (P = 0.001) and the psychosocial sub- and 63.4 ± 14.6, respectively, before the interventions, and
scales (P = 0.01) at the end of the intervention (Table 2). six and twelve weeks after it; also, in the Frenkel group,
the mean fatigue at these aforementioned times was 89.6
There was a statistically significant reduction in the ± 16.4, 84.3 ± 16.6, and 78.6 ± 16.3, respectively. Fatigue
mean score of total fatigue of the two exercise groups; in was not reduced in the control group, and it gradually in-
other words, both interventions reduced fatigue in the pa- creased according to the FIS score from 89.2 ± 15.5 at base-
tients. However, the reduction of fatigue was statistically line to 96.5 ± 18 at the end of the study.
significant in vestibular rehabilitation exercise in compar-

4 Iran Red Crescent Med J. In Press(In Press):e68913.


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Karami F et al.

Furthermore, a difference in the mean scores of to- this study, there was a correlation between increasing bal-
tal fatigue was observed in both the vestibular rehabilita- ance and decreasing fatigue. The effect of vestibular reha-
tion and the Frenkel group in comparison with the control bilitation exercise on improving various symptoms, such
group, at the end of the intervention (P = 0.001). The dif- as dizziness, quality of life (41), and balance (42) in MS pa-
ferences in the mean scores of total fatigue in the vestibu- tients and also reducing the risk of falls in older adults (43)
lar rehabilitation group in comparison with the control have been reported. On the other hand, the positive ef-
group, six and twelve weeks after intervention, were 14.1, fect of Frenkel exercise for elderly individuals as well as for
and 33.1, respectively; in the Frenkel group, however, the patients with neurological disorders associated with im-
differences were 8 and 17.9, respectively. balances was reported in a study by Makuła (44). Increas-
Additionally, the findings showed that there was a bal- ing fatigue in the control group of the current study in-
ance in the improvement of exercise groups after the in- dicated that the lack of a planned exercise program may
tervention (P = 0.001). Therefore, correlational analyses lead to worsening of symptoms in patients with MS. The
were performed to test the relationship between fatigue other result of the current study showed that vestibular re-
and balance. The Pearson correlation coefficient test was habilitation exercise was more effective than Frenkel exer-
used for the analysis of associations; a negative correlation cise. This finding had a number of similarities with the re-
between fatigue and balance was reported at the end of the sults of Hebert et al., they showed that MS patients, who
intervention phase (r = -0.5, P < 0.001). participated in vestibular rehabilitation exercise experi-
enced decreased fatigue than the exercise control group
and the wait listed control group (45). Vestibular rehabil-
5. Discussion itation exercises can affect three balance centers (i.e. the
cerebellum, vestibular, and the visual system) at the same
The effectiveness of vestibular rehabilitation and time (46, 47). This can result in improving balance, and
Frenkel exercise on fatigue were compared among MS subsequently, further fatigue reduction. Frenkel exercise
patients in the present study. The results showed that may only improve the cerebellum function for coordinat-
fatigue decreased in MS patients following the mentioned ing movements (48).
exercises and the vestibular rehabilitation exercise was According to another finding of the current study,
more effective in decreasing fatigue in comparison to the there were differences in the reductions of fatigue in the
Frenkel exercise. physical and psychosocial subscales between the two exer-
Consistent with available studies about the effective- cises, yet no difference was observed in the cognitive sub-
ness of exercise therapy, Kierkegaard et al. (35), and Giesser scale. The treatment of cognitive fatigue is very complex
(36) reported reduced fatigue in MS patients following dif- as a variety of factors may be involved in its origin (49),
ferent exercise therapies. How exercises decrease fatigue and it has a negative effect on cognitive tasks, physical con-
in MS patients is still poorly understood, however, the rea- ditions, and social functions (50). Therefore, treatments
son behind this decrease may be due to the effect of exer- should target to improve cognitive fatigue in MS patients.
cises in increasing energy reserves and enhancing neuro- Although the findings of this study are related to the
biological processes (37). In addition, environmental phys- positive effects of vestibular rehabilitation and Frenkel ex-
iology changes, such as increasing oxygen and blood sup- ercise on fatigue in MS patients, some limitations need
ply to muscles that occur after exercise, may be effective in to be considered. The first limitation was the data collec-
reducing fatigue (38). In contrast to the current findings, tion tool. Although the reliability and the validity of the
a study by Pilutti et al. showed that supported treadmill FIS has been approved in Persian, being a self-report ques-
training had a low impact on decreasing fatigue in MS pa- tionnaire in addition to the subjective nature of fatigue
tients (39). Furthermore, Newman et al. found that the might have an influence on the accuracy of patients to an-
level of fatigue in MS patients was unchanged after aerobic swer questions. Therefore, further studies are suggested
training (40). Results contradicting the aforementioned to examine the effectiveness of these exercises with other
phenomenon may be due to the type and the duration of fatigue measures, particularly with more objective tools.
exercises, methodology of the studies, and the various fa- The second limitation of this study was that the majority
tigue assessment tools. of patients in this study had the relapsing-remitting type
Patients in the current study experienced a reduction of MS. Since fatigue may be different in the four types of
in fatigue following both exercise programs in comparison MS (relapsing-remitting, secondary-progressive, primary-
to the control group. The reason for this finding may be progressive, and progressive-relapsing), further studies
due to the effect of these exercises on improving the pa- are recommended to investigate the effects of the men-
tient’s balance; therefore, they can reduce fatigue. As in tioned exercises on fatigue in MS patients with the other

Iran Red Crescent Med J. In Press(In Press):e68913. 5


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Karami F et al.

forms of the disease. 3. Fox RJ, Bacon TE, Chamot E, Salter AR, Cutter GR, Kalina JT, et al. Preva-
In summary, the current study showed that both lence of multiple sclerosis symptoms across lifespan: Data from the
NARCOMS registry. Neurodegener Dis Manag. 2015;5(6 Suppl):3–10. doi:
vestibular rehabilitation and Frenkel exercise could re-
10.2217/nmt.15.55. [PubMed: 26611264].
duce fatigue at the end of the exercises, however, there 4. Induruwa I, Constantinescu CS, Gran B. Fatigue in multiple
were significant differences in the effects of these exer- sclerosis: A brief review. J Neurol Sci. 2012;323(1-2):9–15. doi:
cises. In other words, the vestibular rehabilitation exercise 10.1016/j.jns.2012.08.007. [PubMed: 22935407].
5. Newland PK, Lunsford V, Flach A. The interaction of fatigue, physical
is more effective than the Frenkel exercise in reducing fa- activity, and health-related quality of life in adults with multiple scle-
tigue. Finally, the researchers suggest that these exercises rosis (MS) and cardiovascular disease (CVD). Appl Nurs Res. 2017;33:49–
should be performed alongside medication in MS patients 53. doi: 10.1016/j.apnr.2016.09.001. [PubMed: 28096022].
owing to their various benefits, such as ease of learning, 6. Thompson AJ, Toosy AT, Ciccarelli O. Pharmacological management
of symptoms in multiple sclerosis: Current approaches and fu-
low cost, and non-invasive nature. ture directions. Lancet Neurol. 2010;9(12):1182–99. doi: 10.1016/S1474-
4422(10)70249-0. [PubMed: 21087742].
7. Kunkel A, Fischer M, Faiss J, Dahne D, Kohler W, Faiss JH. Impact
Supplementary Material of natalizumab treatment on fatigue, mood, and aspects of cogni-
tion in relapsing-remitting multiple sclerosis. Front Neurol. 2015;6:97.
Supplementary material(s) is available here [To read
doi: 10.3389/fneur.2015.00097. [PubMed: 26029156]. [PubMed Central:
supplementary materials, please refer to the journal web- PMC4426783].
site and open PDF/HTML]. 8. Tur C. Fatigue management in multiple sclerosis. Curr Treat Op-
tions Neurol. 2016;18(6):26. doi: 10.1007/s11940-016-0411-8. [PubMed:
27087457]. [PubMed Central: PMC4834309].
Acknowledgments 9. Mackay AM, Buckingham R, Schwartz RS, Hodgkinson S, Beran RG,
Cordato DJ. The effect of biofeedback as a psychological intervention
The authors wish to thank all MS patients for their kind in multiple sclerosis: A randomized controlled study. Int J MS Care.
participation in this research study. The researchers, also 2015;17(3):101–8. doi: 10.7224/1537-2073.2014-006. [PubMed: 26052255].
[PubMed Central: PMC4455862].
thank the Office of Vice Chancellor for Research at Yasuj
10. van den Akker LE, Beckerman H, Collette EH, Eijssen IC, Dekker J,
University of Medical Sciences, and those, who guided and de Groot V. Effectiveness of cognitive behavioral therapy for the
helped the study. treatment of fatigue in patients with multiple sclerosis: A system-
atic review and meta-analysis. J Psychosom Res. 2016;90:33–42. doi:
10.1016/j.jpsychores.2016.09.002. [PubMed: 27772557].
Footnotes 11. Langeskov-Christensen M, Bisson EJ, Finlayson ML, Dalgas U. Potential
pathophysiological pathways that can explain the positive effects of
Authors’ Contribution: Fatemeh Karami: designing exercise on fatigue in multiple sclerosis: A scoping review. J Neurol Sci.
the research, sampling, allocating samples to the study 2017;373:307–20. doi: 10.1016/j.jns.2017.01.002. [PubMed: 28131211].
12. Peruzzi A, Cereatti A, Della Croce U, Mirelman A. Effects of a vir-
groups, implementation of the intervention, collecting
tual reality and treadmill training on gait of subjects with multi-
data, and compiling the article; Ardashir Afrasiabifar: ple sclerosis: A pilot study. Mult Scler Relat Disord. 2016;5:91–6. doi:
monitoring of intervention, analysis of data, and compil- 10.1016/j.msard.2015.11.002. [PubMed: 26856951].
ing the article, and Shahla Najafi Doulatabad: collecting 13. Scheidler A, Tisha A, Kinnett-Hopkins D, Learmonth Y, Motl R, López-
Ortiz C. Targeted dance program for improved mobility in multiple
data.
sclerosis. In: Ibá-ez JGVJ, Azorín J, Akay M, Pons J, editors. Converging
Conflict of Interests: None declared. clinical and engineering research on neurorehabilitation. Biosystems &
Biorobotics: Springer, Cham; 2017. p. 1073–7.
Ethical Considerations: The Ethics Committee Approval
14. Tallner A, Waschbisch A, Hentschke C, Pfeifer K, Maurer M. Mental
Number: ir.yums.REC.1394.180. health in multiple sclerosis patients without limitation of physical
Funding/Support: This study was supported by a Master function: The role of physical activity. Int J Mol Sci. 2015;16(7):14901–
11. doi: 10.3390/ijms160714901. [PubMed: 26147422]. [PubMed Central:
thesis grant from the Deputy of Research and Technology
PMC4519878].
of the Yasuj University of Medical Sciences, Iran. 15. Kerling A, Keweloh K, Tegtbur U, Kuck M, Grams L, Horstmann
H, et al. Effects of a short physical exercise intervention on pa-
tients with multiple sclerosis (MS). Int J Mol Sci. 2015;16(7):15761–75.
References doi: 10.3390/ijms160715761. [PubMed: 26184173]. [PubMed Central:
PMC4519923].
1. Rudroff T, Kindred JH, Ketelhut NB. Fatigue in multiple sclerosis: Mis-
16. Nortvedt MW, Riise T, Maeland JG. Multiple sclerosis and lifestyle fac-
conceptions and future research directions. Front Neurol. 2016;7:122.
tors: The hordaland health study. Neurol Sci. 2005;26(5):334–9. doi:
doi: 10.3389/fneur.2016.00122. [PubMed: 27531990]. [PubMed Central:
10.1007/s10072-005-0498-2. [PubMed: 16388368].
PMC4969300].
17. Motl RW, McAuley E, Snook EM. Physical activity and multi-
2. Hadjimichael O, Vollmer T, Oleen-Burkey M; North American Re-
ple sclerosis: A meta-analysis. Mult Scler. 2005;11(4):459–63. doi:
search Committee on Multiple Sclerosis. Fatigue characteristics
10.1191/1352458505ms1188oa. [PubMed: 16042230].
in multiple sclerosis: The North American Research Commit-
tee on Multiple Sclerosis (NARCOMS) survey. Health Qual Life Out-
comes. 2008;6:100. doi: 10.1186/1477-7525-6-100. [PubMed: 19014588].
[PubMed Central: PMC2596785].

6 Iran Red Crescent Med J. In Press(In Press):e68913.


Uncorrected Proof

Karami F et al.

18. Latimer-Cheung AE, Pilutti LA, Hicks AL, Martin Ginis KA, Fenuta 35. Kierkegaard M, Lundberg IE, Olsson T, Johansson S, Ygberg S, Opava
AM, MacKibbon KA, et al. Effects of exercise training on fitness, C, et al. High-intensity resistance training in multiple sclerosis - An
mobility, fatigue, and health-related quality of life among adults exploratory study of effects on immune markers in blood and cere-
with multiple sclerosis: A systematic review to inform guideline brospinal fluid, and on mood, fatigue, health-related quality of life,
development. Arch Phys Med Rehabil. 2013;94(9):1800–1828 e3. doi: muscle strength, walking and cognition. J Neurol Sci. 2016;362:251–7.
10.1016/j.apmr.2013.04.020. [PubMed: 23669008]. doi: 10.1016/j.jns.2016.01.063. [PubMed: 26944158].
19. Heine M, van de Port I, Rietberg MB, van Wegen EE, Kwakkel G. Exercise 36. Giesser BS. Exercise in the management of persons with mul-
therapy for fatigue in multiple sclerosis. Cochrane Database Syst Rev. tiple sclerosis. Ther Adv Neurol Disord. 2015;8(3):123–30. doi:
2015;(9). CD009956. doi: 10.1002/14651858.CD009956.pub2. [PubMed: 10.1177/1756285615576663. [PubMed: 25941539]. [PubMed Central:
26358158]. PMC4409551].
20. Geddes EL, Costello E, Raivel K, Wilson R. The effects of a twelve-week 37. White LJ, Castellano V. Exercise and brain health–implications
home walking program on cardiovascular parameters and fatigue for multiple sclerosis: Part 1–neuronal growth factors. Sports
perception of individuals with multiple sclerosis: A pilot study. Car- Med. 2008;38(2):91–100. doi: 10.2165/00007256-200838020-00001.
diopulm Phys Ther J. 2009;20(1):5–12. [PubMed: 20467528]. [PubMed [PubMed: 18201113].
Central: PMC2845260]. 38. Kileff J, Ashburn A. A pilot study of the effect of aerobic exercise
21. Shepard NT, Telian SA, Smith-Wheelock M. Quociente da sensibilidade on people with moderate disability multiple sclerosis. Clin Rehabil.
motora Ltda. In: Herdman SJ, editor. Reabilitação vestibular. 20. São 2005;19(2):165–9. doi: 10.1191/0269215505cr839oa. [PubMed: 15759531].
Paulo: Editora Manole; 2002. 364 p. 39. Pilutti LA, Lelli DA, Paulseth JE, Crome M, Jiang S, Rathbone MP, et al.
22. Szturm T, Ireland DJ, Lessing-Turner M. Comparison of different ex- Effects of 12 weeks of supported treadmill training on functional abil-
ercise programs in the rehabilitation of patients with chronic pe- ity and quality of life in progressive multiple sclerosis: A pilot study.
ripheral vestibular dysfunction. J Vestibul Res. 1994;4(6):461–79. doi: Arch Phys Med Rehabil. 2011;92(1):31–6. doi: 10.1016/j.apmr.2010.08.027.
10.3233/VES-1994-4606. [PubMed: 21187202].
23. Corna S, Nardone A, Prestinari A, Galante M, Grasso M, Schieppati M. 40. Newman MA, Dawes H, van den Berg M, Wade DT, Burridge J, Izadi
Comparison of Cawthorne-Cooksey exercises and sinusoidal support H. Can aerobic treadmill training reduce the effort of walking and
surface translations to improve balance in patients with unilateral fatigue in people with multiple sclerosis: A pilot study. Mult Scler.
vestibular deficit. Arch Phys Med Rehabil. 2003;84(8):1173–84. [PubMed: 2007;13(1):113–9. doi: 10.1177/1352458506071169. [PubMed: 17294619].
12917857]. 41. Pavan K, Marangoni BE, Schmidt KB, Cobe FA, Matuti GS, Nishino
24. Michael KM, Allen JK, Macko RF. Fatigue after stroke: Relationship LK, et al. [Vestibular rehabilitation in patients with relapsing-
to mobility, fitness, ambulatory activity, social support, and falls ef- remitting multiple sclerosis]. Arq Neuropsiquiatr. 2007;65(2A):332–5.
ficacy. Rehabil Nurs. 2006;31(5):210–7. [PubMed: 16948443]. Portuguese. [PubMed: 17607438].
25. Moreira KLdAF, Dornelas L, Tavares GR, Andrade SM. Physical therapy 42. Afrasiabifar A, Karami F, Najafi Doulatabad S. Comparing the effect
intervention and acquired immunodeficiency syndrome associated of Cawthorne-Cooksey and Frenkel exercises on balance in patients
to leukoencephalopathy and neurotoxoplasmosis: Case’s relate. Fi- with multiple sclerosis: A randomized controlled trial. Clin Rehabil.
sioterapia em Movimento. 2007;20(3):35–40. 2018;32(1):57–65. doi: 10.1177/0269215517714592. [PubMed: 28629268].
26. Steib S, Zech A, Hentschke C, Pfeifer K. Fatigue-induced alterations of 43. Ribeiro Ados S, Pereira JS. Balance improvement and reduction of
static and dynamic postural control in athletes with a history of ankle likelihood of falls in older women after Cawthorne and Cooksey ex-
sprain. J Athl Train. 2013;48(2):203–8. doi: 10.4085/1062-6050-48.1.08. ercises. Braz J Otorhinolaryngol. 2005;71(1):38–46. [PubMed: 16446890].
[PubMed: 23672384]. [PubMed Central: PMC3600922]. 44. Makuła W. Rola i zastosowanie ćwiczeń Frenkla w rehabilitacji ru-
27. Hebert JR, Corboy JR. The association between multiple sclerosis- chowej. Antropomotoryka. 2013;1(23):29–36.
related fatigue and balance as a function of central sensory integra- 45. Hebert JR, Corboy JR, Manago MM, Schenkman M. Effects of vestibular
tion. Gait Posture. 2013;38(1):37–42. doi: 10.1016/j.gaitpost.2012.10.015. rehabilitation on multiple sclerosis-related fatigue and upright pos-
[PubMed: 23200463]. tural control: A randomized controlled trial. Phys Ther. 2011;91(8):1166–
28. Van Emmerik RE, Remelius JG, Johnson MB, Chung LH, Kent-Braun 83. doi: 10.2522/ptj.20100399. [PubMed: 21680771].
JA. Postural control in women with multiple sclerosis: Effects of task, 46. Cohen HS, Kimball KT. Increased independence and decreased
vision and symptomatic fatigue. Gait Posture. 2010;32(4):608–14. doi: vertigo after vestibular rehabilitation. Otolaryngol Head Neck Surg.
10.1016/j.gaitpost.2010.09.002. [PubMed: 20943393]. 2003;128(1):60–70. doi: 10.1067/mhn.2003.23. [PubMed: 12574761].
29. Ministry of Health and Medical Education (MOHME); Iran Univer- 47. Saini S, DeStefano N, Smith S, Guidi L, Amato MP, Federico A, et al.
sity of Medical Sciences (IUMS). Iranian Registry of Clinical Trials (IRCT). Altered cerebellar functional connectivity mediates potential adap-
2018. Available from: http://en.search.irct.ir/view/29230. tive plasticity in patients with multiple sclerosis. J Neurol Neurosurg
30. Cawthorne T. [The physiological basis for head exercises]. J Char Soc Psychiatry. 2004;75(6):840–6. [PubMed: 15145996]. [PubMed Central:
Physiother. 1944;3:106–7. Japanese. PMC1739042].
31. Cooksey FS. Rehabilitation in vestibular injuries. Proc R Soc Med. 48. Zwecker M, Zeilig G, Ohry A. Professor heinrich sebastian frenkel:
1946;39(5):273–8. [PubMed: 19993269]. [PubMed Central: PMC2181739]. A forgotten founder of rehabilitation medicine. Spinal Cord.
32. Ojoga F, Marinescu S. Physical therapy and rehabilitation for ataxic 2004;42(1):55–6. doi: 10.1038/sj.sc.3101515. [PubMed: 14713947].
patients. Balneo Res. 2013;4(2):81–4. doi: 10.12680/balneo.2013.1044. 49. Sandry J, Genova HM, Dobryakova E, DeLuca J, Wylie G. Subjective
33. Fisk JD, Pontefract A, Ritvo PG, Archibald CJ, Murray TJ. The im- cognitive fatigue in multiple sclerosis depends on task length. Front
pact of fatigue on patients with multiple sclerosis. Can J Neurol Sci. Neurol. 2014;5:214. doi: 10.3389/fneur.2014.00214. [PubMed: 25386159].
1994;21(1):9–14. [PubMed: 8180914]. [PubMed Central: PMC4209827].
34. Heidari M, Akbarfahimi M, Salehi M, Nabavi SM. [Validity and reliabil- 50. Schwartz CE, Coulthard-Morris L, Zeng Q. Psychosocial correlates of
ity of the Persian-version of fatigue impact scale in multiple sclerosis fatigue in multiple sclerosis. Arch Phys Med Rehabil. 1996;77(2):165–70.
patients in Iran]. Koomesh. 2014;15(3):295–301. Persian. [PubMed: 8607741].

Iran Red Crescent Med J. In Press(In Press):e68913. 7


8
Table 1. Between Group Comparisons of Mean Scores of Patients’ Fatiguea

Groups Vestibular Rehabilitation Frenkel Control P Value


(Time/Group)

Change Scores Change Scores Change Scores


95% Confidence Interval for Mean 95% Confidence Interval for Mean 95% Confidence Interval for Mean Repeated
from from from
Fatigue/Times Mean ± SD Mean ± SD Mean ± SD Measures
Baseline, Baseline, Baseline,
ANOVA
Mean (SD) Lower Bound Upper Bound Mean (SD) Lower Bound Upper Bound Mean (SD) Lower Bound Upper Bound

Total fatigue

T1 92.7 ± 12.8 - 86.6 98.8 89.6 ± 16.4 - 83.4 95.8 89.2 ± 15.5 - 83.2 95.1

T2 78.2 ± 15.2 -14.5 (3.4) 71.6 84.8 84.3 ± 16.6 -5.3 (2.4) 77.6 91 92.3 ± 16.5 3.1 (2.2) 85.9 98.8 0.001

T3 63.4 ± 14.6 -29.3 (4.30 56.8 70.1 78.6 ± 16.3 -11 (2.1) 71.7 85.4 96.5 ± 18 7.3 (4.5) 90 103.1

Cognitive subscale

T1 20.4 ± 3.5 - 18.8 21.9 22.5 ± 4.1 - 20.9 24.1 19.7 ± 4 - 18.2 21.3

T2 18.7 ± 3.3 -1.7 (1.4) 17.4 20.1 20.2 ± 3.5 -2.3 (1.4) 18.8 21.6 20.8 ± 3.6 1.1 (1.3) 19.5 22.2 0.001

T3 16.3 ± 3.4 -4.1 (2.2) 14.8 17.7 17.9 ± 3.6 -4.6 (1.9) 16.4 19.4 22 ± 3.6 2.3 (1.9) 20.5 23.4

Physical subscale

T1 28.3 ± 4.8 - 26 30.7 27.8 ± 5.5 - 25.4 30.2 26.6 ± 6.9 - 24.3 29

T2 21.2 ± 4.7 -7.1 (2.4) 18.9 23.6 25.9 ± 5.3 -1.9 (1.7) 23.5 28.3 27.4 ± 6.7 0.8 (1.1) 25.1 29.7 0.01

T3 14.4 ± 4.6 -13.9 (2.7) 12.3 16.6 23.8 ± 4.5 -4 (1.9) 21.6 26 28.8 ± 6.4 2.2 (1.7) 26.7 30.9
Karami F et al.

Psychosocial subscale

T1 44 ± 9.7 - 39.7 48.3 39.3 ± 11.5 - 34.9 43.6 42.8 ± 10.1 - 38.6 47

T2 38.2 ± 10 -5.8 (2.3) 33.9 42.5 38.2 ± 11.3 -1.1 (1.2) 33.7 42.6 44.1 ± 10.7 1.3 (1.2) 39.8 48.3 0.001

T3 27.9 ± 6.6 -16.1 (3.8) 23.8 32.1 36.9 ± 11.3 -2.4 (1.3) 32.7 41.1 45.8 ± 11.5 3 (2.4) 41.7 49.8
Uncorrected Proof

a T1, baseline; T2, six weeks after starting the intervention; T3, twelve weeks after starting the intervention.

Iran Red Crescent Med J. In Press(In Press):e68913.


Table 2. Paired Comparison of the Mean Differences of Patients’ Fatigue by Time/Group

Paired Comparison Vestibular Rehabilitation-Frenkel Vestibular Rehabilitation-Control Frenkel-Control

95% CI for Mean Difference 95% CI for Mean Difference 95% CI for Mean Difference
Fatigue/Times Mean Difference P Valuea Mean Difference P Valuea Mean Difference P Valuea
Lower Bound Upper Bound Lower Bound Upper Bound Lower Bound Upper Bound

Total fatigue

T2 -6.1 -17.6 5.4 0.4 -14.1 -25.4 2.8 0.009 -8 -19.4 3.4 0.2

T3 -15.2 -26.8 -3.4 0.007 -33.1 -44.6 -21.6 0.001 -17.9 -29.6 -6.3 0.001

Cognitive subscale

T2 -1.5 -3.9 1 0.1 -2.1 -4.5 0.3 0.09 -0.6 -3.1 1.8 0.8

T3 -1.6 -4.2 0.9 0.1 -5.7 -8.1 -3.2 0.001 -4.1 -6.6 -1.5

Physical subscale

T2 -4.7 -8.7 -0.6 0.01 -6.2 -10.1 -2.1 0.001 -1.5 -5.5 2.5 0.6

T3 -9.4 -13.1 -5.5 0.001 -14.4 -18 -10.6 0.001 -5 -8.8 -1.3 0.005

Psychosocial
subscale

T2 0 -7.6 7.6 0.9 -5.9 -13.3 1.6 0.1 -5.9 -13.5 1.7 0.1

T3 -9 -16.1 -1.7 0.01 -17.9 -24.9 -10.7 0.001 -8.9 -16 -1.7 0.009

Iran Red Crescent Med J. In Press(In Press):e68913.


Abbreviation: CI, confidence interval.
a Post Hoc.
Karami F et al.
Uncorrected Proof

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